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Pollen limitation and its effect on seed germination

Published online by Cambridge University Press:  25 July 2018

Jerry M. Baskin  and
Carol C. Baskin
Jerry M. Baskin
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY 40506-0225, USA
Carol C. Baskin*
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY 40506-0225, USA Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546-0312, USA
*
Author for correspondence: Carol C. Baskin, Email: [email protected]
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Abstract

In nature, fruit and seed production in many plants have been shown to be pollen limited. Pollen limitation is demonstrated when open-pollinated plants that are hand-supplemented (Ps) with outcross pollen produce more fruits and/or seeds than open-pollinated controls that are not hand-pollinated (Po). There are three categories of results in such studies: Ps > Po, Ps = Po and Ps < Po, in which case pollen limitation indices are positive, zero and negative, respectively. In an index widely used to calculate pollen limitation, 1 – (Po/Ps), the bounds for Ps ≥ Po are 0 to + 1, whereas the bounds for Ps < Po are 0 to –∞. The first aim of this review was to show how the pollen limitation index can be modified so that the bounds of Ps < Po are 0 and –1, whereupon the index gives equal weight to the best performer (Ps or Po) and worst performer (Ps or Po). In addition to seed quantity, pollen supplementation can affect seed quality, including germinability. Thus, our second aim was to summarize the results of studies that have also tested the effect of pollen limitation on seed germination. In short, the 30 case studies in 15 families, 16 genera and 18 species that we identified show that seed germination percentage increased, was not affected or decreased by pollen supplementation in 12, 11 and seven cases, respectively. The effect of pollen limitation on seed germination, which can be quite large, has not been considered in developing population growth models to determine the effect of pollen limitation on λ.

Keywords

open pollinationpollen limitation indicespopulation growth rate (λ)seed germinationsupplemental pollination
Type
Research Opinion
Information
Seed Science Research , Volume 28 , Issue 4 , December 2018 , pp. 253 - 260
Copyright
Copyright © Cambridge University Press 2018 

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References

Aguilar, R and Bernardello, G (2001) The breeding system of Lycium cestroides: a Solanaceae with ovarian self-incompatibilty. Sexual Plant Reproduction 13, 273–277.Google Scholar
Aizen, MA and Harder, LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88, 271–281.Google Scholar
Ashman, T-L, Knight, TM, Steets, JA, Amarasekare, P, Burd, M, Campbell, DR, Dudash, MR, Johnston, MO, Mazer, SJ, Mitchell, RJ, Morgan, MT and Wilson, WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 2408–2421.Google Scholar
Asikainen, E and Mutikainen, P (2005) Pollen and resource limitation in a gynodioecious species. American Journal of Botany 92, 487–494.Google Scholar
Baskin, JM and Baskin, CC (2000) Evolutionary considerations of claims for physical dormancy-break by microbial action and abrasion by soil particles. Seed Science Research 10, 409–413.Google Scholar
Baskin, JM and Baskin, CC (2015a) Pollen (microgametophyte) competition: an assessment of its significance in the evolution of flowering plant diversity, with particular reference to seed germination. Seed Science Research 25, 1–11.Google Scholar
Baskin, JM and Baskin, CC (2015b) Inbreeding depression and the cost of inbreeding on seed germination. Seed Science Research 25, 355–385Google Scholar
Baskin, JM and Baskin, CC (2017) Seed germination in cleistogamous species: theoretical considerations and a literature survey of experimental results. Seed Science Research 27, 84–98.Google Scholar
Bewley, JD, Bradford, KJ, Hilhorst, HWM and Nonogaki, H (2013) Seeds: Physiology of Development, Germination and Dormancy (3rd edn). New York: Springer.Google Scholar
Bierzychudek, P (1981) Pollination limitation of plant reproductive effort. The American Naturalist 117, 838–840.Google Scholar
Bierzychudek, P (1982) The demography of jack-in-the pulpit, a forest perennial that changes sex. Ecological Monographs 52, 335–351.Google Scholar
Bond, WJ (1994) Do mutualisms matter: assessing the impact of pollinator and disperser disruption on plant extinction. Philosophical Transactions of the Royal Society of London B 344, 83–90.Google Scholar
Brown, E and Kephart, S (1999) Variability in pollen load: implications for reproduction and seedling vigor in a rare plant, Silene douglasii var. oraria. International Journal of Plant Sciences 16, 1145–1152.Google Scholar
Burd, M (1994) Bateman's principle and plant reproduction: the role of pollen limitation in fruit and seed set. The Botanical Review 60, 83–139.Google Scholar
Byers, DL (1995) Pollen quantity and quality as explanations for low seed set in small populations exemplified by Eupatorium (Asteraceae). American Journal of Botany 82, 1000–1006.Google Scholar
Campbell, LG and Husband, BC (2007) Small populations are mate-poor but pollinator-rich in a rare, self-incompatible plant, Hymenoxys herbacea (Asteraceae). New Phytologist 174, 915–925.Google Scholar
Castro, S, Silveira, P and Navarro, L (2008) How flower biology and breeding system affect the reproductive success of the narrow endemic Polygala vayredae Costa (Polygalaceae). Botanical Journal of the Linnean Society 157, 67–81.Google Scholar
Clark, CJ, Poulsen, JR, Levey, DJ and Osenberg, CW (2007) Are plant populations seed limited? A critique and meta-analysis of seed addition experiments. The American Naturalist 170, 128–142.Google Scholar
Colling, G, Reckinger, C and Matthies, D (2004) Effects of pollen quantity and quality on reproduction and offspring vigor in the rare plant Scorzonera humilis (Asteraceae). American Journal of Botany 9, 1774–1782.Google Scholar
Cursach, J and Rita, J (2012) Reproductive biology of Ranunculus weyleri (Ranunculaceae), a narrowly endemic plant from the Balearic Islands with disjunct populations. Flora 207, 726–735.Google Scholar
Delmas, CEL, Escaravage, N, Cheptou, P-O, Charrier, O, Ruzafa, S, Winterton, P and Pornon, A (2014) Relative impact of mate versus pollinator availability on pollen limitation and outcrossing rates in a mass-flowering species. Plant Biology 17, 209–218.Google Scholar
Dogterom, MH, Winston, ML and Mukai, A (2000) Effect of pollen load size and source (self, cross) on seed and fruit production in highbush blueberry cv. ‘Bluecrop’ (Vaccinium corymbosum; Ericaceae). American Journal of Botany 87, 1584–1591.Google Scholar
Duan, Y-W, Zhang, T-F and Liu, J-Q (2007) Interannual fluctuations in floral longevity, pollinator visitation and pollination limitation of an alpine plant (Gentiana straminea Maxim., Gentianaceae) at two altitudes in the Qinghai-Tibetan Plateau. Plant Systematics and Evolution 267, 255–265.Google Scholar
Eckert, CG, Kalisz, S, Geber, MA, Sargent, R, Elle, E, Cheptou, P-O, Goodwillie, C, Johnston, MO, Kelly, JK, Moeller, DA, Porcher, E, Ree, RH, Vallejo-Marín, M and Winn, AA (2010) Plant mating systems in a changing world. Trends in Ecology and Evolution 25, 35–43.Google Scholar
Ehrlén, and Eriksson, O (1995) Pollen limitation and population growth in a herbaceous perennial legume. Ecology 76, 652–656.Google Scholar
Ferrer, MM, Good-Avila, SV, Montana, C, Dominguez, CA and Eguiarte, LE (2009) Effect of variation in self-incompatibility on pollen limitation and inbreeding depression in Flourensia cernua (Asteraceae) scrubs of contrasting density. Annals of Botany 103, 1077–1089.Google Scholar
Garcia, MB and Ehrlén, J (2002) Reproductive effort and herbivory timing in a perennial herb: fitness components at the individual and population levels. American Journal of Botany 89, 1295–1302.Google Scholar
Garcia-Camacho, R and Totland, O (2009) Pollen limitation in the alpine: a meta-analysis. Arctic, Antarctic, and Alpine Research 41, 103–111.Google Scholar
Gargano, D, Fenu, G and Bernardo, L (2017) Local shifts in floral biotic interactions in habitat edges and their effects on quantity and quality of plant offspring. AoB Plants 9, plx031.Google Scholar
González-Varo, JP, Arroyo, J and Aparicio, A (2009) Effects of fragmentation on pollinator assemblage, pollen limitation and seed production of Mediterranean myrtle (Myrtus communis). Biological Conservation 142, 1058–1065.Google Scholar
González-Varo, JP and Traveset, A (2010) Among-individual variation in pollen limitation and inbreeding depression in a mixed-mating shrub. Annals of Botany 106, 999–1008.Google Scholar
Hegland, SJ and Totland, Ø (2007) Pollen limitation affects progeny vigour and subsequent recruitment in the insect-pollinated herb Rananculus acris. Oikos 116, 1204–1210.Google Scholar
Hill, LM, Brody, AK and Tedesco, CL (2008) Mating strategies and pollen limitation in a globally threatened perennial Polemonium vanbruntiae. Acta Oecologica 33, 314–323.Google Scholar
Holland, JN, Bronstein, JL and DeAngelis, DL (2004) Testing hypotheses for excess flower production and low fruit-to-flower ratios in a pollinating seed-consuming mutualism. Oikos 105, 633–640.Google Scholar
Holm, S-O (1994) Reproductive variability and pollen limitation in three Betula taxa in northern Sweden. Ecography 17, 73–81.Google Scholar
Hove, AA, Mazer, SJ and Ivey, CT (2016) Seed set variation in wild Clarkia populations: teasing apart the effects of seasonal resource depletion, pollen quality, and pollen quantity. Ecology and Evolution 6, 6524–6536.Google Scholar
Jacquemart, A-L (1997) Pollen limitation in three sympatric species of Vaccinium (Ericaceae) in the Upper Ardennes, Belgium. Plant Systematics and Evolution 207, 159–172.Google Scholar
Joosen, RVL, Kodde, J, Willems, LAJ, Ligterink, W, van der Plas, LHW and Hilhorst, HWM (2010) GERMINATOR: a software package for high-throughput scoring and curve fitting of Arabidopsis seed germination. The Plant Journal 62, 148–159.Google Scholar
Jules, ES and Rathcke, BJ (1999) Mechanisms of reduced Trillium recruitment along edge of old-growth forest fragments. Conservation Biology 13, 784–793.Google Scholar
Kasagi, T and Kudo, G (2003) Variations in bumble bee preference and pollen limitation among neighboring populations: comparisons between Phyllodoce caerulea and Phyllodoce aleutica (Ericaceae) along snowmelt gradients. American Journal of Botany 90, 1321–1327.Google Scholar
Kelly, D, Ladley, JJ and Robertson, AW (2007) Is the pollen-limited mistletoe Peraxilla tetrapetala (Loranthaceae) also seed limited? Austral Ecology 32, 850–857.Google Scholar
Kelly, D, Ladley, JJ, Robertson, AW, Anderson, SH, Wotton, DM and Wiser, SK (2010) Mutualisms with the wreckage of an avifauna: the status of bird pollination and fruit-dispersal in New Zealand. New Zealand Journal of Ecology 34, 66–85.Google Scholar
Knight, TM (2004) The effects of herbivory and pollen limitation on a declining population of Trillium grandiflorum. Ecological Monographs 14, 915–928.Google Scholar
Knight, TM, Steets, JA and Ashman, T-L (2006) A quantitative synthesis of pollen supplementation experiments highlights the contribution of resource reallocation to estimates of pollen limitation. American Journal of Botany 93, 271–277.Google Scholar
Knight, TM, Steets, JA, Vamosi, JC, Mazer, SJ, Burd, M, Campbell, DR, Dudash, MR, Johnston, MO, Mitchell, RJ and Ashman, T-L (2005) Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution, and Systematics 36, 467–497.Google Scholar
Larson, BMH and Barrett, SCH (1999) The ecology of pollen limitation in buzz-pollinated Rhexia virginica (Melastomataceae). Journal of Ecology 87, 371–381.Google Scholar
Larson, BMH and Barrett, SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biological Journal of the Linnean Society 69, 503–520.Google Scholar
Law, W, Salick, J and Knight, TM (2010) The effects of pollen limitation on population dynamics of snow lotus (Saussurea medusa and S. laniceps, Asteraceae): threatened Tibetan medicinal plants of the eastern Himalayas. Plant Ecology 210, 343–357.Google Scholar
Lázaro, A and Traveset, A (2006) Reproductive success of the endangered shrub Buxus balearica Lam. (Buxaceae): pollen limitation, and inbreeding and outbreeding depression. Plant Systematics and Evolution 261, 117–128.Google Scholar
Lehtila, K and Syrjänen, K (1995) Positive effects of pollination on subsequent size, reproduction, and survival of Primula veris. Ecology 76, 1084–1098.Google Scholar
Lienert, J and Fischer, M (2004) Experimental inbreeding reduces seed production and germination independent of fragmentation of populations of Swertia perennis. Basic and Applied Ecology 5, 43–52.Google Scholar
Liu, H and Koptur, S (2003) Breeding system and pollination of a narrowly endemic herb of the lower Florida Keys: impacts of the urban-wildland interface. American Journal of Botany 90, 1180–1187.Google Scholar
Marten-Rodriguez, S and Fenster, CB (2010) Pollen limitation and reproductive assurance in Antillean Gesneriaceae: a specialist vs. generalist comparison. Ecology 91, 155–165.Google Scholar
Merrett, MF, Robertson, AW and Peterson, PG (2007) Pollination performance and vulnerability to pollination breakdown of sixteen native shrub species from New Zealand. New Zealand Journal of Botany 45, 579–591.Google Scholar
Moeller, DA (2004) Facilitative interactions among plants via shared pollinators. Ecology 85, 3289–3301.Google Scholar
Moeller, DA, Geber, MA, Eckhart, VM and Tiffin, P (2012) Reduced pollinator service and elevated pollen limitation at the geographic range limit of an annual plant. Ecology 93, 1036–1048.Google Scholar
Montgomery, RR, Kelly, D and Ladley, JJ (2001) Pollination limitation of seed set in Fuchsia perscandens (Onagraceae) on Banks Peninsula, South Island, New Zealand. New Zealand Journal of Botany 39, 559–565.Google Scholar
Navarro, L and Guitián, J (2002) The role of floral biology and breeding system on the reproductive success of the narrow endemic Petrocoptis viscosa Rothm. (Caryophyllaceae). Biological Conservation 103, 125–132.Google Scholar
Parker, IM (1997) Pollinator limitation of Cystisus scoparius (scotch broom), an invasive exotic shrub. Ecology 78, 1457–1470.Google Scholar
Parker, MA (1987) Pathogen impact on sexual vs. asexual reproductive success in Arisaema triphyllum. American Journal of Botany 74, 1758–1763.Google Scholar
Pico, FX and Retana, J (2003) Seed ecology of a Mediterranean perennial herb with an exceptionally extended flowering and fruiting season. Botanical Journal of the Linnean Society 142, 273–280.Google Scholar
Price, MV, Campbell, DR, Waser, NM and Brody, AK (2008) Bridging the generation gap in plants: pollination, parental fecundity, and offspring demography. Ecology 89, 1596–1604.Google Scholar
Primack, RB and Hall, P (1990) Costs of reproduction in the pink Lady's slipper orchid: a four-year experimental study. The American Naturalist 135, 638–656.Google Scholar
Ramsey, M (1995) Causes and consequences of seasonal variation in pollen limitation of seed production in Blandfordia grandiflora (Liliaceae). Oikos 73, 49–58.Google Scholar
Ramsey, M (1997) No evidence of demographic costs of seed production in the pollen-limited perennial herb Blandfordia grandiflora (Liliaceae). International Journal of Plant Sciences 158, 785–793.Google Scholar
Ramsey, M and Vaughton, G (2000) Pollen quality limits seed set in Burchardia umbellate (Colchicaceae). American Journal of Botany 87, 846–852.Google Scholar
Robertson, AW, Kelly, D and Ladley, JJ (2011) Futile selfing in the trees Fuchsia excorticata (Onagraceae) and Sophora microphylla (Fabaceae): inbreeding depression over 11 years. International Journal of Plant Sciences 172, 191–198.Google Scholar
Robertson, AW, Ladley, JJ, Kelly, D, McNutt, KL, Peterson, PG, Merrett, MF and Karl, BJ (2008) Assessing pollination and fruit dispersal in Fuchsia excorticate (Onagracaee). New Zealand Journal of Botany 46, 299–314.Google Scholar
Shabir, PA, Nawchoo, IA, Wani, AA and Banday, A (2015) Pollen limitation and effects of local patch density on reproductive success in the alpine herb Inula royleana (Asteraceae). Plant Ecology 216, 1073–1081.Google Scholar
Snow, AA and Whigham, DR (1989) Costs of flower and fruit production in Tipularia discolor (Orchidaceae). Ecology 70, 1286–1293.Google Scholar
Soltani, E, Ghaderi-Far, F, Baskin, CC and Baskin, JM (2015) Problems with using mean germination time to calculate rate of seed germination. Australian Journal of Botany 63, 631–635.Google Scholar
Spigler, RB and Chang, S-M (2009) Pollen limitation and reproduction varies with population size in experimental populations of Sabatia angularis (Gentianaceae). Botany 87, 330–338.Google Scholar
Suarez-Gonzalez, A and Good, SV (2014) Pollen limitation and reduced reproductive success are associated with local genetic effects in Prunus virginiana, a widely distributed self-incompatible shrub. Annals of Botany 113, 595–605.Google Scholar
Tamura, S and Kudo, G (2000) Wind pollination and insect pollination of two temperate willow species, Salix miyabeana and Salix sachalinensis. Plant Ecology 147, 185–192.Google Scholar
Van Etten, ML, Tate, JA, Anderson, SH, Kelly, D, Ladley, JJ, Merrett, MF, Peterson, PG and Robertson, AW (2015) The compounding effects of high pollen limitation, selfing rates and inbreeding depression leave a New Zealand tree with few viable offspring. Annals of Botany 116, 833–843.Google Scholar
Vanhoenacker, D, Ågren, J and Ehrlén, J (2006) Spatio-temporal variation in pollen limitation and reproductive success of two scape morphs of Primula farinosa. New Phytologist 169, 615–621.Google Scholar
Ward, M and Johnson, SD (2005) Pollen limitation and demographic structure in small fragmented populations of Brunsvigia radulosa (Amaryllidaceae). Oikos 108, 253–262.Google Scholar
Wolf, AT and Harrison, SP (2001) Effects of habitat size and patch isolation on reproductive success of the serpentine morning glory. Conservation Biology 15, 111–121.Google Scholar
Young, HJ and Young, TP (1992) Alternative outcomes of natural and experimental high pollen loads. Ecology 73, 639–647.Google Scholar
Zalamea, PC, Sarmineto, C, Arnold, AE, Davis, AS and Dalling, JW (2015) Do soil microbes and abrasion by soil particles influence persistence and loss of physical dormancy in seeds of tropical pioneers. Frontiers in Plant Science 5 (article 799), 1–13.Google Scholar
Zimmerman, M and Pyke, GH (1988) Reproduction in Polemonium: assessing the factors limiting seed set. The American Naturalist 131, 723–738.Google Scholar